Dieter Ebert

Virulence and Local Adaptation of a Horizontally Transmitted Parasite

Parasites are thought to maximize the number of successfully transmitted offspring by trading off propagule production against host survival. In a horizontally transmitted microparasitic disease in Daphnia, a planktonic crustacean, increasing geographic distance between host and parasite origin was found to be correlated with a decrease in spore production and virulence. This finding indicates local adaptation of the parasite, but contradicts the hypothesis that long-standing coevolved parasites are less virulent than novel parasites. Virulence can be explained as the consequence of balancing the positive genetic correlation between host mortality and strain-specific spore production.

GENETIC VARIATION IN A HOST-PARASITE ASSOCIATION: POTENTIAL FOR COEVOLUTION AND FREQUENCY-DEPENDENT SELECTION

Abstract.— Models of host‐parasite coevolution assume the presence of genetic variation for host resistance and parasite infectivity, as well as genotype‐specific interactions. We used the freshwater crustacean Daphnia magna and its bacterial microparasite Pasteuria ramosa to study genetic variation for host susceptibility and parasite infectivity within each of two populations. We sought to answer the following questions: Do host clones differ in their susceptibility to parasite isolates? Do parasite isolates differ in their ability to infect different host clones? Are there host clone‐parasite isolate interactions? The analysis revealed considerable variation in both host resistance and parasite infectivity. There were significant host clone‐parasite isolate interactions, such that there was no single host clone that was superior to all other clones in the resistance to every parasite isolate. Likewise, there was no parasite isolate that was superior to all other isolates in infectivity to every host clone. This form of host clone‐parasite isolate interaction indicates the potential for coevolution based on frequency‐dependent selection. Infection success of original host clone‐parasite isolate combinations (i.e., those combinations that were isolated together) was significantly higher than infection success of novel host clone‐parasite isolate combinations (i.e., those combinations that were created in the laboratory). This finding is consistent with the idea that parasites track specific host genotypes under natural conditions. In addition, correspondence analysis revealed that some host clones, although distinguishable with neutral genetic markers, were susceptible to the same set of parasite isolates and thus probably shared resistance genes.

Host–parasite ‘Red Queen’ dynamics archived in pond sediment

Antagonistic interactions between hosts and parasites are a key structuring force in natural populations, driving coevolution. However, direct empirical evidence of long-term host–parasite coevolution, in particular ‘Red Queen’ dynamics—in which antagonistic biotic interactions such as host–parasite interactions can lead to reciprocal evolutionary dynamics—is rare, and current data, although consistent with theories of antagonistic coevolution, do not reveal the temporal dynamics of the process. Dormant stages of both the water flea Daphnia and its microparasites are conserved in lake sediments, providing an archive of past gene pools. Here we use this fact to reconstruct rapid coevolutionary dynamics in a natural setting and show that the parasite rapidly adapts to its host over a period of only a few years. A coevolutionary model based on negative frequency-dependent selection, and designed to mimic essential aspects of our host–parasite system, corroborated these experimental results. In line with the idea of continuing host–parasite coevolution, temporal variation in parasite infectivity changed little over time. In contrast, from the moment the parasite was first found in the sediments, we observed a steady increase in virulence over time, associated with higher fitness of the parasite.

On the evolutionary ecology of specific immune defence

Abstract Evolutionary ecology has developed along two major conceptual avenues, starting from the observation that hosts vary in their immune defence against parasites The first avenue, rooted in life-history theory, assumes fitness costs of immune defence and tradeoffs in the face of limited resources, rather than specific host–parasite interactions. The second avenue focuses on specific responses, especially those generated by genotype–genotype interaction between and within host and parasite species. Specificity in the interactions between hosts and parasites play a crucial role in the field but analysis is difficult. Here, we classify concepts about host–parasite interactions into these two families and discuss their reconciliation with the help of a defence component model and two-dimensional classification scheme of the individual components. This helps to clarify some of the confusing terminology and might guide further research in the field.

Challenging the trade-off model for the evolution of virulence: is virulence management feasible?

Progress in understanding the evolution of infectious diseases has inspired proposals to manage the evolution of pathogen (including parasite) virulence. A common view is that social interventions that lower pathogen transmission will indirectly select lower virulence because of a trade-off between transmission and virulence. Here, we argue that there is little theoretical justification and no empirical evidence for this plan. Although a trade-off model might apply to some pathogens, the mechanism appears too weak for rapid selection of substantial changes in virulence. Direct selection against virulence itself might be a more rewarding approach to managing the evolution of virulence.

The evolution of parasitic diseases

Parasites are characterized by their fitness-reducing effect on their hosts. Studying the evolution of parasitic diseases is an attempt to understand these negative effects as an adaptation of the parasite, the host, both or neither. Dieter Ebert and E. Allen Herre here discuss how the underlying concepts are general and are applicable for all types of disease-producing organisms, broadly defined here as parasites. The evolutionary processes that lead to the maintenance of the harmful effects are believed to be characterized by genetic correlations with other fitness components of the parasite. Depending on the shape of these correlations, any level of virulence can evolve.

The Population Dynamics of Vertically and Horizontally Transmitted Parasites

We analyse a model of the transmission dynamics of a parasite transmitted both vertically and horizontally. The basic reproductive ratio (R0) of the parasite is shown to be a sum of horizontal and vertical components. We derive expressions for the equilibrium prevalence of infection for a mixture of horizontal and vertical transmission; prevalence can reach 100% if transmission is sufficiently high. At the endemic equilibrium, if prevalence is high, most transmission will in general be vertical, but horizontal transmission rates must be high to reach and stably maintain such an equilibrium. Surprisingly, for such parasites the highest equilibrium rates of vertical transmission are observed when horizontal transmission is very effective. We discuss the implications for assessing the importance of horizontal v. vertical transmission from field data, and we suggest some implications for the evolution of virulence.

The Effect of Parasites on Host Population Density and Extinction: Experimental Epidemiology with Daphnia and Six Microparasites

Parasites have been shown to reduce host density and to induce host population extinction in some cases but not in others. Epidemiological models suggest that variable effects of parasites on individual hosts can explain this variability on the population level. Here, we aim to support this hypothesis with a specific epidemiological model using a cross‐parasite species approach. We compared the effect of six parasites on host fecundity and survival to their effects on density and risk of extinction of clonal host populations. We contrast our empirical results of population density with predictions from a deterministic model and contrast our empirical results of host and parasite extinction rates with those predicted by a stochastic model. Five horizontally transmitted microparasites (two bacteria: white bacterial disease, Pasteuria ramosa; two microsporidia: Glugoides intestinalis, Ordospora colligata; one fungus: Metschnikowiella biscuspidata); and six strains of a vertically transmitted microsporidium (Flabelliforma magnivora) of the planktonic crustacean Daphnia magna were used. In life table experiments, we quantified fecundity and survival in individual parasitized and healthy hosts and compared these with the effect of the parasites on host population density and on the likelihood of host population extinction in microcosm populations. Parasite species varied strongly in their effects on host fecundity, host survival, host density reduction, and the frequency with which they drove host populations to extinction. The fewer offspring an infected host produced, the lower the density of an infected host population. This effect on host density was relatively stronger for the vertically transmitted parasite strains than for the horizontally transmitted parasites. As predicted by the stochastic simulations, strong effects of a parasite on individual host survival and fecundity increased the risk of host population extinction. The same was true for parasite extinctions. Our results have implications for the use of microparasites in biological control programs and for the role parasites play in driving small populations to extinction.

Within–and between–population variation for resistance of Daphnia magna to the bacterial endoparasite Pasteuria ramosa

Genetic variation among hosts for resistance to parasites is an important assumption underlying evolutionary theory of host and parasite evolution. Using the castrating bacterial parasite Pasteuria ramosa and its cladoceran host Daphnia magna, we examined both within– and between–population genetic variation for resistance. First, we tested hosts from four populations for genetic variation for resistance to three parasite isolates. Allozyme analysis revealed significant host population divergence and that genetic distance corresponds to geographic distance. Host and parasite fitness components showed strong genetic differences between parasite isolates for host population by parasite interactions and for clones within populations, whereas host population effects were significant for only a few traits. In a second experiment we tested explicitly for within–population differences in variation for resistance by challenging nine host clones from a single population with four different parasite spore doses. Strong clone and dose effects were evident. More susceptible clones also suffered higher costs once infected. The results indicate that within–population variation for resistance is high relative to between–population variation. We speculate that P. ramosa adapts to individual host clones rather than to its host population.

The Evolution of Virulence When Parasites Cause Host Castration and Gigantism

It has been suggested that the harm parasites cause to their hosts is an unavoidable consequence of parasite reproduction with costs not only for the host but also for the parasite. Castrating parasites are thought to minimize their costs by reducing host fecundity, which may minimize the chances of killing both host and parasite prematurely. We conducted a series of experiments to understand the evolution of virulence of a castrating bacterium in the planktonic crustacean Daphnia magna. By manipulating food levels during the infection of D. magna with the bacterium Pasteuria ramosa, we showed that both antagonists are resource‐limited and that a negative correlation between host and parasite reproduction exists, indicating resource competition among the antagonists. Pasteuria ramosa also induces enhanced growth of its hosts (gigantism), which we found to be negatively correlated with host fecundity but positively correlated with parasite reproduction. Because infected hosts never recovered from infections, we concluded that gigantism is beneficial only for the parasite. Hosts, however, have evolved counteradaptations. We showed that infected hosts have enhanced reproduction before castration. This shift to earlier reproduction increases overall host fecundity and compromises parasite reproduction. Finally, we showed that this resource conflict is subject to genetic variation among host and parasite genotypes within a population and is therefore likely to be an important force in the coevolution of virulence in this system. A verbal model is presented and suggests that the adaptive value of gigantism is to store host resources, which are liberated after parasitic castration for later use by the growing parasite. This hypothesis assumes that infections are long lasting, that is, that they have a high life expectancy.